bioRxiv preprint doi: https://doi.org/10.1101/556456; this version posted February 21, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license.

Adult emergence order in a community of cavity-nesting and , and

their parasites

J Scott MacIvor

Department of Biological Science, University of Toronto Scarborough, 1265 Military Trail,

Toronto, Ontario, Canada M1C 1A4

email: [email protected]

phone: +1-416-208-8191

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Abstract

Evaluating resource use and overlap through time and space among and within species having

similar habitat requirements informs community-level conservation and coexistence, efforts to

monitor species at-risk and biological invasions. Many species share common nesting

requirements; one example are cavity-nest bees and wasps, which provision nests in dark and dry

holes in wood, plant stems, or other plant-based materials that can be bundled together into ‘trap

nests’. In this study, the adult emergence order of 47 species of solitary cavity-nesting bees and

wasps, and their parasites (total N>8000 brood cells) were obtained from two hundred identical

trap nests set up each year (over three years) to survey these populations across Toronto, Canada

and the surrounding region. All brood cells collected were reared in a growth chamber under

constant warming temperature and humidity to determine species identity, and adult emergence

order. This order ranged from 0 to 38 days, with all mason bees (Osmia spp.) emerging within

the first two days, and the invasive resin species, sculpturalis Smith significantly

later than all others. Late emerging species i) exhibited significantly greater intraspecific

variation in mean emergence day and ii) were significantly larger in body size, compared to early

emerging species. Detailing natural history information at the species- and community-level,

such as the adult emergence order of coexisting cavity-nesting bees and wasps and their

parasites, can inform the timing of deployment of trap nests to support and monitor target

species, and refine experimental design to study these easily-surveyed and essential

communities.

Keywords: ; Osmia; Megachile; nest box; trap nest; interspecific variation; niche

partitioning; host-parasite interactions

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Introduction

Interspecific partitioning in the timing of similar, critical life-history stages is an evolutionary

adaptation used to minimize resource overlap and competition among species (Richards 1927;

Schoener 1974; Albrecht and Gotelli 2001; Martin et al. 2004; Taylor et al. 2014). For example,

many nest provisioning solitary bee and species share similar nesting location preferences,

yet have evolved to partition these resources in order to coexist in time (Wcislo and Cane 1996;

Hoehn et al. 2008) and space (Willmer and Corbet 1981; Tylianakis et al. 2005). Intraspecific

variation at these critical life-history stages can also be important in determining fitness among

individuals within the same species (Bolnick et al. 2011). Variation in emergence from nests as

adults may be linked to evolutionary adaptations to local environmental conditions that optimize

reproductive and foraging success. In temperate regions, solitary bees and wasps are active for

short overlapping periods in a season, which are linked to the availability of preferred resources

(Lindsey 1958; Minckley et al. 1994; Leong and Thorp 1999). The remainder of the year is spent

as an immature in a nest constructed by the mother (with some exceptions).

Considerable information is available from field and laboratory studies on the lifecycle,

incubation period, and adult emergence order of specific solitary bee species managed for

pollination in agriculture, such as Osmia lignaria Say (Bosch et al. 2000), Osmia cornifrons

(Radoszkowski) (White et al. 2009), or (Fabricius) (Tepedino and Parker

1986). However, there are relatively little data on community-wide adult emergence order or

knowledge of intraspecific variation in emergence order of most coexisting solitary bees, and

especially wasps, many of which are important predators in biological communities (Budrienė et

al. 2004; Forrest and Thomson 2011; Fründ et al. 2013). Many solitary bee and wasp species

provision nests in cavities above ground (e.g. pithy or hollowed out plant stems, beetle-bored

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holes in wood), hereafter ‘cavity-nesting bees and wasps’ (Stephen and Osgood 1965; Bohart

1972; Williams et al. 2010). For many cavity-nesting species, artificial nests that represent the

natural nesting conditions can be made by gathering ‘nesting tubes’ (e.g. drilled holes in wood,

plant stems, or paper cardboard tubes) together, commonly referred to as ‘trap nests’ (Figure 1)

(Krombein 1967). Trap nests are widely used to survey cavity-nesting bees and wasps, and their

parasites, which include cleptoparasitic bees and wasps, as well as parasitoid wasps, flies, and

beetles (Tscharntke et al. 1998; Praz et al. 2008; MacIvor 2017). Identifying nests occurring

naturally in the landscape is time consuming and difficult to retrieve in sufficient numbers

needed for experiments. On the other hand, rearing cavity-nesting bees and wasps, and their

parasites to adulthood from individuals obtained from nesting tubes in trap nests is a useful way

to identify species-level interactions and community-level patterns at a local or landscape scale

(Staab et al. 2018). Many other studies utilize trap nests to evaluate relationships between species

diversity and resource utilization, and in response to environmental change (Yocum et al. 2005;

Sheffield et al. 2008; O’Neill et al. 2011; Fliszkiewicz et al. 2012; Fründ et al. 2013). There are

applications as well; for example, to support species of concern, the addition of foraging plants

(Sheffield et al. 2008) or accelerate the release of bees reared on mass to synchronize with target

crops (Bosch et al. 2000).

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Figure 1. A trap nest used to study cavity-nesting bees and wasps. The cardboard paper ‘nesting tubes’ are inserted into a piece of pink insulation board fitted into a white PVC pipe for support and protection from rain.

In this study, the adult emergence order among and within 47 coexisting species of

cavity-nesting bees and wasps, and their parasites were quantified from individuals obtained

from trap nests and reared in a laboratory setting at constant temperature and humidity, to

represent a spring warming period. The main objective was to map emergence order in this

community of cavity-nesting bees and wasps, and their parasites to improve management of

these important taxa, for example, to 1) support an abundance of target species, 2) aid in the

detection of invasive species, or 3) monitor host-parasite interactions as environmental

indicators.

Using these data, I also evaluate two hypotheses. First, that intraspecific variation in

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emergence time will increase in late emerging species because they incubate longer than early

emerging species, and fluctuations in the environment can affect development time (O’Neill et

al. 2011). Second, although Bosch and Kemp (2002) noted no relationship between intraspecific

body size and adult emergence in the European Orchard bee, Osmia cornuta, I predicted body

size differences between species in the bee and wasp community would affect interspecific adult

emergence order, with larger bodied species emerging significantly later than smaller bodied

species, because body size is generally correlated with development time to adult (Garcia-Barros,

2000).

Methods

The cavity-nesting bees and wasps, and their parasites examined here were obtained from a

survey of 200 trap nests set up each year (one per site) from May to October for three years

(2011-2013) throughout the city of Toronto and surrounding region. The sites were a minimum

250m apart and spread over an area encompassing approximately 745km2. Trap nests were made

of white PVC piping that was 10cm in diameter and 28cm in length, a circular faceplate made of

insulation board into which 30 cardboard nesting tubes (Custom Paper Tubes, Cleveland, OH)

were inserted (10 of each of three tube diameters; 3.4mm, 5.5mm, 7.6mm; all 15cm in length) at

one end, and the opposite end was blocked with a PVC pipe cap (Figure 1). Each year, in

October, trap nests were collected, each cardboard nesting tube opened, and every brood cell

removed. The contents of each brood cell were labeled with a unique identifier and placed into

individual cells within 24-cell assay trays with the lid on. A complete incubation process

includes a sufficiently long cooling period (Bosch and Kemp 2004), and so all specimens spent

the cold season (October – March) in a walk-in fridge kept at a constant 4°C (as in Bosch et al.

2000).

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At the end of the cold season, in early April the following year, the assay trays containing

all brood cells from the previous year were moved from the walk-in fridge to a sealed growth

chamber where temperature and humidity were held constant at 26°C and 60% (Johansen and

Eves 1973; Tepedino and Parker 1986). All species overwintered as prepupae (mature post-

defecated larvae) except for mason bees (Osmia spp.), and a parasite wasp of Osmia (Sapyga

centrata Say) which overwinter as adults. The growth chamber was windowless and kept dark

for the duration of the study except when lights were turned on during daily inspection of brood

cells to measure adult emergence order (as in Sheffield et al. 2008). Approximately 3% of all

cells in the growth chamber were lost to parasitic wasps (Melittobia chalybii Ashmead and

Monodontomerus obscurus Westwood) wasps that emerged early and attacked other larvae still

undergoing development. To reduce their depredations, four traps, each consisting of a black

light and a bowl filled with water and dish soap, were set up to attract and reduce the number of

these minute wasps that emerged and escaped the assay tray (Eves et al. 1980). For each

individual bee, wasp, or parasite, the time to emergence was recorded as the number of days

from the start of warming (e.g. onset of the incubation period) to the time of development to

adulthood and emergence from the cocoon (Owen and McCorquodale 1994; Sheffield et al.

2008). After the three-year survey, a total of 84 species of bee, wasp, and parasite were identified

(MacIvor and Packer 2015), but emergence day was recorded for only those species with 5 or

more successfully emerged adults with timing accurately recorded, and so 47 species and 8,006

individuals were used for this study (Figure 2). All bees, wasps, and parasites were identified

using the collections from the Packer Lab at York University and the Marshall Lab at University

of Guelph. All specimens are kept in the MacIvor Lab at University of Toronto Scarborough.

An analysis of variance (α=0.05) was used to determine if there was a significant

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difference in interspecific adult emergence order (in days post onset of incubation) among the

cavity-nesting bees and wasps, and their parasites. Given my objectives, all males and females

per species were grouped together; even though males emerge on average slightly earlier than

females, both sexes emerge near the same time to ensure reproduction. A tukey-post hoc analysis

was then conducted to evaluate significant differences among species of bee, wasp, and parasite.

A Pearson’s R correlation was used to examine whether the intraspecific variation in emergence

day, as determined by the standard error of the mean, increased with increasing mean emergence

day across the community. Finally, the intertegular (IT) span (Cane 1987; Greenleaf et al. 2007;

Williams et al. 2010) was measured (in mm) using an ocular micrometer attached to a dissecting

microscope on a sample of 5–10 individuals per species and a linear regression was used to

compare IT and mean emergence day among all species. All statistics were completed using the

R statistical program v3.2.2 (R Core Team 2015).

Results

Of the 47 species examined, there were 22 species and six genera of bee in two families (all in

the superfamily ). These included bees in the , (), as well as

Osmia, Heriades, Hoplitis, Chelostoma, Megachile (all ). There were 16 species of

cavity-nesting wasp in nine genera and four families, these included Isodontia (Sphecidae),

Passaloecus, and (), as well as , ,

Symmorphus (), and Auplopus and Dipogon (Pompilidae) (Figure 2). Nine species in

seven genera and 5 families of parasites were identified from three orders (Hymenoptera,

Coleoptera, Diptera), and parasites, Ephialtes manifestator (Linnaeus) and Anthrax irroratus Say

had more than one host (Table 1).

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2007 Abd Mean SE sig. Osmia lignaria Say 0.4 0.4 Osmia lignaria Say B 64 0.4 0.4 a

Sapyga centrata Say 0.5 0.4 Sapyga centrata Say P 88 0.5 0.5 a Tax Time Step Osmia pumila Cresson 0.9 0.9 Osmia pumila Cresson B 1,674 0.9 0.9 a Species Rel. Abd. Avg SD a 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 Osmia caerulescens (Linnaeus) + 1.0 1.0 Osmia caerulescens (Linnaeus) + B 924 1.0 1.0 a Osmia lignaria Say B 0.78% 0.4 0.9 0.0 Osmia atriventris Cresson 1.8 1.0 Osmia atriventris Cresson B 18 1.8 1.0 a Sapyga centrata Say P 1.08% 0.5 0.6 Perithous divinator (Rossi) 9 1.247219129 Perithous divinator (Rossi) P 46 9.0 1.2 b Osmia pumila Cresson B 20.46% 0.9 1.0 cuspidatus Smith 10.85714286 3.836610056 Smith W 28 10.9 3.8 bc Osmia caerulescens B 3.78% 1.0 1.7 (Panzer) 12.63131313 2.218372455 Psenulus pallipes (Panzer) + W 594 12.6 2.2 bcde (Linnaeus) + Ephialtes manifestator (Linnaeus) 12.66666667 3.204163958 Ephialtes manifestator (Linnaeus) P 6 12.7 3.2 bcde Osmia atriventris Cresson B 0.22% 1.8 1.0 2.0 Hylaeus annulatus (Linnaeus) 12.93478261 1.79384347 Hylaeus annulatus (Linnaeus) B 46 12.9 1.8 bcdef Perithous divinator (Rossi) P 0.56% 91.247219129 9.0 W 0.34% Dipogon sayi Banks 0 Dipogon sayi Banks W 7 13.0 0.0 cdef Passaloecus cuspidatus 13 10.857142863.836610056 Smith 11.0 Hylaeus affinis Smith 13.55555556 1.846687957 Hylaeus affinis (Smith) B 27 13.6 1.8 cdefg Psenulus meridionalis W 0.29% Trypoxylon frigidum Smith 14.1747851 2.672640546 Trypoxylon frigidum Smith W 698 14.2 2.7 cdefg 11.833333331.203858531 12.0 Beaumont Passaloecus gracilis (Curtis) + 14.99253731 3.414908202 Passaloecus gracilis (Curtis) + W 134 15.0 3.4 defg Psenulus pallipes (Panzer) W 7.26%12.631313132.218372455 12.6 12.6 Ancistrocerus adiabatus (Saussure) 15.36111111 3.243919831 Ancistrocerus adiabatus (Saussure) W 36 15.4 3.2 defgh Ephialtes manifestator P 0.07% 12.666666673.204163958 12.7 12.7 Symmorphus cristatus (Saussure) 15.47840532 2.61732028 Symmorphus cristatus (Saussure) W 301 15.5 2.6 defgh (Linnaeus) B 0.56% (Saussure) 15.66176471 3.276375382 Euodynerus foraminatus (Saussure) W 68 15.7 3.3 defghi Hylaeus annulatus 12.934782611.79384347 13.0 12.9 12.9 12.9 (Linnaeus) Euodynerus planitarsis (Bohart) 15.77777778 4.816061092 Euodynerus planitarsis (Bohart) W 9 15.8 4.8 defghi Dipogon sayi Banks W 0.09% 13 0 13.0 13.0 13.0 auratus (Linnaeus) + 15.9 1.449137675 (Linnaeus) + W 10 15.9 1.4 efghi Amobia spp. P 0.50%13.121951224.990967451 13.1 13.1 13.1 13.1 Chrysis cembricola Krombein 16.33333333 2.386832566 Chrysis cembricola Krombein P 12 16.3 2.4 efghij Hylaeus affinis Smith B 0.33%13.555555561.846687957 13.6 13.6 13.6 13.6 Hylaeus hylinatus Smith 16.4 2.633122354 Hylaeus hyalinatus Smith + B 10 16.4 2.6 efghij Trypoxylon frigidum Smith W 8.53%14.17478512.672640546 14.0 14.2 14.2 14.2 14.2 Ancistrocerus antilope (Panzer) + 16.49107143 2.478722192 Ancistrocerus antilope (Panzer) + W 112 16.5 2.5 efghij Passaloecus gracilis W 1.64% Symmorphus canadensis (Saussure) 16.88888889 2.821675081 Symmorphus canadensis (Saussure) W 234 16.9 2.8 fghijk 14.992537313.414908202 15.0 15.0 15.0 15.0 (Curtis) + Caenochrysis doriae (Gribodo) 1.772810521 Caenochrysis doriae (Gribodo) P 8 17.0 1.8 ghijkl 17 Ancistrocerus adiabatus W 0.44% 15.361111113.243919831 15.4 15.4 15.4 15.4 15.4 Smith 19.22222222 2.186292344 Megachile frigida Smith B 54 19.2 2.2 hijklm (Saussure) Hoplitis spoliata (Provancher) 19.55434783 2.92906665 Hoplitis spoliata (Provancher) B 92 19.6 2.9 ijklmn Symmorphus cristatus W 3.68% 15.478405322.61732028 15.5 15.5 15.5 15.5 15.5 (Saussure) Auplopus mellipes (Say) 20.68 3.4607321 Auplopus mellipes (Say) W 25 20.7 3.5 klmnop Euodynerus foraminatus W 0.83% Caenochrysis tridens (Lepeletier) 4.707021647 Caenochrysis tridens (Lepeletier) P 84 20.8 4.7 klmnopq 15.661764713.276375382 15.7 15.7 15.7 15.7 15.7 15.7 20.80952381 (Saussure) Cresson 20.87878788 1.218543592 Megachile relativa Cresson B 33 20.9 1.2 lmnopq Euodynerus planitarsis W 0.11% 15.777777784.816061092 16.0 15.8 15.8 15.8 15.8 15.8 (Linnaeus) 20.90540541 2.312995491 Megachile centuncularis (Linnaeus) + B 444 20.9 2.3 lmnopq (Bohart) Heriades carinata Cresson 21.37254902 2.926472533 Heriades carinata Cresson B 153 21.4 2.9 mnopqr Auplopus carbonarius W 0.07% 15.833333330.98319208 15.8 15.8 15.8 15.8 15.8 (Scopoli) + Chelostoma rapunculi (Lepeletier) 22.26785714 1.623588298 Chelostoma rapunculi (Lepeletier) + B 56 22.3 1.6 mnopqr Pseudomalus auratus W 0.12% Nemognatha piazata (Fabricius) 23 0 Nemognatha piazata (Fabricius) P 5 23.0 0.0 mnopqr 15.91.449137675 15.9 15.9 15.9 15.9 15.9 (Linnaeus) + Provancher 23.18181818 1.622354657 Megachile inermis Provancher B 22 23.2 1.6 nopqr Chrysis cembricola P 0.15% 16.333333332.386832566 16.3 16.3 16.3 16.3 16.3 16.3 Isodontia mexicana (Saussaure) 23.5678392 2.600343966 Isodontia mexicana (Saussaure) W 199 23.6 2.6 opqrs Krombein

Hoplitis producta (Cresson) 24 1.236693885 Hoplitis producta (Cresson) B 52 24.0 1.2 pqrst Hylaeus hylinatus Smith B 0.12% 16.42.633122354 16.4 16.4 16.4 16.4 16.4 16.4 Cresson 24 1.414213562 Megachile mendica Cresson B 5 24.0 1.4 pqrst Ancistrocerus antilope W 1.37% 16.491071432.478722192 16.5 16.5 16.5 16.5 16.5 16.5 (Panzer) + Hyaleus modestus Say 24.71428571 0.755928946 Hylaeus modestus Say B 7 24.7 0.8 qrstu Symmorphus canadensis W 2.86% Chelostoma campanularum (Kirby) 25.07692308 2.985005261 Chelostoma campanularum (Kirby) + B 13 25.1 3.0 rstuv 16.888888892.821675081 16.9 16.9 16.9 16.9 16.9 16.9 (Saussure) Anthrax irroratus Say 25.2 2.863564213 Anthrax irroratus Say P 5 25.2 2.9 rstuvw Caenochrysis doriae P 0.10% 171.772810521 17.0 17.0 17.0 17.0 17.0 17.0 (Robertson) 27.33819242 3.281513735 Megachile campanulae (Robertson) B 343 27.3 3.3 stuvw (Gribodo)

Megachile rotundata Fabricius 27.53805774 3.230079909 Megachile rotundata (Fabricius) + B 381 27.5 3.2 tuvw Megachile frigida Smith B 0.66%19.222222222.186292344 19.2 19.2 19.2 19.2 19.2 19.2 Trypoxylon collinum Smith 28.51593323 2.428485557 Trypoxylon collinum Smith W 659 28.5 2.4 uvw Hoplitis spoliata B 1.12% 19.554347832.92906665 19.6 19.6 19.6 19.6 19.6 19.6 (Provancher) Say 28.72164948 2.230201168 Megachile pugnata Say B 97 28.7 2.2 vwx Physocephala marginata P 0.04% Sapyga louisi Krombein 29.14925373 3.897371808 Sapyga louisi Krombein P 67 29.1 3.9 wx 202.645751311 (Say) 20.0 20.0 20.0 20.0 20.0 20.0 Trypoxylon lactitarse Saussure 32.62328767 1.955153794 Trypoxylon lactitarse Saussure W 146 32.6 2.0 x Auplopus mellipes (Say) W 0.31% 20.683.4607321 20.7 20.7 20.7 20.7 20.7 20.7 Smith 37.4 0.699205899 Megachile sculpturalis Smith + B 10 37.4 0.7 y 0 5 10 15 20 25 30 35 40 Caenochrysis tridens P 1.03% 20.809523814.707021647 (Lepeletier) 20.8 20.8 20.8 20.8 20.8 20.8 20.8 Mean Day of Emergence (+/- SE) Megachile relativa Cresson B 0.40%20.878787881.218543592 20.9 20.9 20.9 20.9 20.9 20.9 B 5.43% Megachile centuncularis 20.905405412.312995491 (Linnaeus) 20.9 20.9 20.9 20.9 20.9 20.9 Heriades carinata Cresson B 1.87%21.372549022.926472533 21.4 21.4 21.4 21.4 21.4 21.4 Figure 2. Variation in the mean emergence time for species of bee, wasp, and parasite recorded from B 0.68% Chelostoma rapunculi 22.267857141.623588298 (Lepeletier) 22.3 22.3 22.3 22.3 22.3 22.3 Nemognatha piazata P 0.02% 23 0 23.0 23.0 23.0 23.0 23.0 23.0 individuals taken from trap nests. ‘Taxa’ denotes cavity-nesting bees (B), cavity-nesting wasps (W), and (Fabricius) Megachile inermis B 0.27% 23.181818181.622354657 parasites (P). ‘Abd’ is the total number of individuals incubated and emerged successfully. ‘Mean’ is the Provancher 23.2 23.2 23.2 23.2 23.2 Isodontia mexicana W 2.43% 23.56783922.600343966 23.6 23.6 23.6 23.6 23.6 (Saussaure) average number of days taken to emerge and ‘SE’ is the standard error of the mean. Significant Hoplitis producta (Cresson) B 0.64% 241.236693885 24.0 24.0 24.0 24.0 24.0 Megachile mendica B 0.06% 241.414213562 24.0 24.0 24.0 24.0 24.0 differences between species (‘sig’) were given alphabetically where species sharing a letter were not Cresson Hyaleus modestus Say B 0.09%24.714285710.755928946 24.7 24.7 24.7 24.7 24.7 Chelostoma B 0.16% 25.076923082.985005261 25.1 25.1 25.1 25.1 25.1 significantly different from one another (α = 0.05). Those species denoted with a “+” are considered campanularum (Kirby) Anthrax irroratus Say P 0.06% 25.22.863564213 25.2 25.2 25.2 25.2 25.2 25.2 Megachile campanulae B 4.19% introduced to the region. 27.338192423.281513735 27.3 27.3 27.3 27.3 27.3 (Robertson) Megachile rotundata B 4.66% 27.538057743.230079909 Fabricius 27.5 27.5 27.5 27.5 Trypoxylon collinum Smith W 8.06%28.515933232.428485557 28.5 28.5 28.5 Interspecific mean emergence day (e.g. number of incubation days to adulthood) among Megachile pugnata Say B 1.19%28.721649482.230201168 28.7 28.7 28.7 Sapyga louisi Krombein P 0.82%29.149253733.897371808 29.2 29.2 Trypoxylon lactitarse W 1.78% 32.623287671.955153794 Saussure 32.6 Megachile sculpturalis B 0.12% all 47 species was significantly different (F47=786.29, p<0.001) and ranged from 0 to 38 (Figure 37.40.699205899 37.4 Smith

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2). Many significant differences were noted. For example, the data confirmed one anticipated

pattern, that mason bees (Osmia spp.) emerge significantly earlier than all others because they

overwinter as adults (Fye 1965; Bosch et al. 2001) (Figure 2). The invasive large resin bee,

Megachile sculpturalis, was the largest species recorded in this study and emerged significantly

later than all other species (average emergence day = 37.4±0.7 days; mean±SE) (Figure 2). The

greatest overlap (e.g. average emergence day did not differ significantly) occurred between day

12 and 17, when 15 species (three cavity-nesting bees, ten cavity-nesting wasps, and two

parasites) emerged (Figure 2).

Parasites had significantly higher variation in adult emergence than both cavity-nesting

bees and wasps (F2=4.190, p=0.021). The difference in the mean emergence day between

parasite and host varied depending on the parasite species. For example, the parasitic fly, A.

irroratus emerged on average 25 days after its host, whereas emergence day of three cuckoo

wasps were more similar to that of their host: on average, Chrysis cembricola Krombein

emerged on the same day as Symmorphus canadensis (de Saussure), Caenochrysis doriae

(Gribodo) emerged 2.8 days later than its host Trypoxylon frigidum Smith, and Caenochrysis

tridens (Lepeletier) emerged 7.7 days earlier than its host Trypoxylon collinum Smith (Figure 2).

Late emerging species exhibited greater intraspecific variation in emergence day. A

Pearson’s R correlation showed there was a significantly positive correlation between mean and

variation in emergence time (Figure 3). Finally, the average emergence time was positively

correlated with body size when all 47 species were included in a linear regression analysis

(Figure 4).

10 bioRxiv preprint doi: https://doi.org/10.1101/556456; this version posted February 21, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license.

Figure 3. Scatterplot illustrating a significantly positive community-wide correlation between intraspecific mean and variation in emergence time.

Figure 4. Scatterplot showing the significant relationship between mean emergence time and body size as measured by the intertegular width.

11 bioRxiv preprint doi: https://doi.org/10.1101/556456; this version posted February 21, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license.

Discussion

There was a significant interspecific difference in average emergence day among the 47 species

of cavity-nesting bees and wasps, and their parasites evaluated. There was evidence to support

both hypotheses, that 1) there would be greater intraspecific variation in emergence day in late

emerging species compared to early emerging species, and 2) late emerging species would be the

largest in body size. Interpreting overlap in emergence time can inform basic knowledge of their

species in communities, but also indirectly, potential competition for nesting resources at trap

nests. These findings can also support action to enhance target species that use trap nests, by, for

example, precisely-timed placement of trap nests in landscapes to increase populations of some

species over others.

Bees in the genus Osmia and one specialist parasite of O. pumila Cresson, the wasp

Sapyga centrata, emerged significantly earlier than all other species (Figure 2). They become

active at the start of spring and this life-history strategy greatly narrow the variation in adult

emergence (Figure 3). The remaining bees, wasps, and parasite species use warming

temperatures as a cue to initiate transition from to adult, a process which is subject to

variation in time to completion due to environmental changes (Tepedino and Parker, 1986; Kemp

and Bosch, 2014). Between day 12 and 17 there was an overlap in the mean emergence day

among ten cavity-nesting wasp species (Figure 2). These wasp species are each predators of a

different group of invertebrates, for example, spiders (Trypoxylon; Medler 1967), caterpillars and

beetle larvae (Symmorphus; Cowan 1981), or (Passoloecus; Fricke 1993). Since these

wasps were similarly sized, competition for nesting locations in this community could be a more

limiting resource than prey opportunities (Wcislo 1996; Potts et al. 2005).

Interspecific body size was positively correlated with mean emergence time and this

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agrees with other comparative studies that show larger take longer to develop (Kingsolver

and Huey, 2008). Cavity-nesting bees and wasps select nesting locations with inner widths that

are closest to their own body width, and so recording interspecific intertegular widths within a

community (see Figure 2) can help practitioners decide on nesting tube dimensions when

implementing trap nests to target specific species of interest and known body sizes (Lee-Mäder

et al. 2010). Late emerging species exhibited greater intraspecific variation than early emerging

species (Figure 3). Being larger can confer a number of benefits; for example, larger bodied

solitary bee species can carry more pollen (e.g. Kendall and Soloman 1973) and larger wasps can

carry larger prey (e.g. O’Neill 1985; Coelho 1997). However, longer periods of time as prepupae

in a nest could increase mortality by parasitism or predation (Stearns and Koella 1986;

Blanckenhorn 2000).

The tropical-in-origin and invasive bee, Megachile sculpturalis, was the largest species

recorded, and the latest to emerge from the nest (Mangum and Sumner 2003). This bee is known

to attack and replace a native bee, Xylocopa virginica (Linnaeus) (Roulston and Malfi 2012), and

likely others coexisting at trap nests. Since M. sculpturalis uses tree resins similar to one

desirable native bee, M. campanulae (Robertson) which emerges significantly earlier

(day=27.2±3.3), M. sculpturalis can be quickly identified and removed due to this 10+ day

difference in emergence time. Knowledge of emergence timing within a community of trap

nesting bees and wasps can therefore finetune temporal applications of strategies for supporting

target species such as monitoring and removal of invasive species.

Parasite-host association and diversity can inform understanding of parasites as indicators

of habitat quality and community-level change (Sheffield et al. 2013). Some authors have noted

that parasites are synchronized with hosts and emerge slightly later relative to them (Thorp et al.

13 bioRxiv preprint doi: https://doi.org/10.1101/556456; this version posted February 21, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license.

1983; Baker et al. 1985). These parasites are typically those that attack and so emerging

after the host ensures host prey is available. For example, in this study the parasitoid Anthrax

irroratus attacked two Osmia species and emerged 25 days after both hosts, at which point he

Osmia females had mated and begun to build nests containing the next generation (Table 1).

Scott and Strickler (1992) also recorded A. irroratus emerging one month after its hosts,

Megachile relativa Cresson and M. inermis Provancher. The parasite larvae develop on the

prepupae of the bee host after hatching from a tiny egg ‘flicked’ indiscriminately into the nest by

the fly as she hovers in front of the nest entrance (Minckley 1989). Each fly larvae overwinter

and develop to adults in the spring (Gerling and Hermann 1976). Cleptoparasites on the other

hand replace the host egg with their own, or their early instar larvae kill the host egg or larva,

and so have an emergence time that is more similar to that of the host (Forrest and Thomson

2011). In this study, cleptoparasites included Chrysis cembricola, Caenochrysis doriae and

Caenochrysis tridens, which all emerged within a week of their host (Figure 2).

Documenting the identity and adult emergence order of coexisting solitary bees, wasps,

and parasites in communities can provide significant information about competition and niche

overlap in these important and ecologically similar taxa (Frankie et al. 1998; Tscharntke et al.

1998; Bosch and Kemp 2002; Tylianakis et al. 2007; Forrest and Thomson 2011). One limitation

of this study is that the emergence times were recorded based on controlled post-incubation

temperature and humidity. More work is needed to examine adult emergence of feral populations

of solitary bees and compare patterns to those obtained from controlled settings (O’Neill et al.

2010).

Solitary cavity-nesting bees and wasps, that i) compete for a common nesting resource,

ii) readily use artificial trap nests, and iii) easily managed by practitioners and citizens intent on

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enhancing their populations and services they provide, are excellent model organisms for

community ecology research, conservation, and outreach with the public on their importance

(Lee-Mäder et al. 2010; Colla and MacIvor 2017). These data on interspecific overlap in nesting

resources can improve initiatives for pollination service management, and a growing number that

are interested in enhancing pest-controlling wasps. Interpreting adult emergence order and

overlap in trap nest communities can also support conservation, for example, by knowing when

to replace nest tubes with fresh empty ones to ensure adequate supply over the season (MacIvor

2017), or for monitoring invasive species requiring control (Barthell et al. 1998). Trap nests

provide a wealth of information on these communities, and so should be in the toolbox of

conservation scientists and practitioners working with these critically important insects.

15 bioRxiv preprint doi: https://doi.org/10.1101/556456; this version posted February 21, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license.

Acknowledgements

Thanks to Baharak Salehi and Jen Albert for help with the incubation and rearing, also Dr.

Laurence Packer and Charlotte de Keyzer for useful comments on the manuscript. Funding was

provided by an NSERC-CGS (CGS D 408565) awarded to the first author, and an NSERC

discovery grant awarded to the supervisor Dr. Laurence Packer.

16 bioRxiv preprint doi: https://doi.org/10.1101/556456; this version posted February 21, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license.

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Table

Table 1. Parasite-host associations determined post-emergence as recorded from trap nests in the

study region over the three years of sampling. ‘Days’ represents the difference in mean

emergence day between the parasite and the host. For parasites having more than one host,

‘Days’ was calculated for each parasite-host pair.

Parasite Family Order Days Hosts Sapyga louisi Krombein Hymenoptera + 7.7 Heriades carinata Sapyga centrata Say Sapygidae Hymenoptera + 0.1 Osmia pumila Ephialtes manifestator (Linnaeus) Hymenoptera - 2.7 Passaloecus gracilis, + 3.1 Passaloecus cuspidatus, - 1.7 Trypoxylon frigidum Perithous divinator (Rossi) Ichneumonidae Hymenoptera - 3.6 Psenulus pallipes Chrysis cembricola Krombein Chrysididae Hymenoptera - 0.6 Symmorphus canadensis Caenochrysis doriae (Gribodo) Chrysididae Hymenoptera + 2.8 Trypoxylon frigidum Caenochrysis tridens (Lepeletier) Chrysididae Hymenoptera - 7.7 Trypoxylon collinum Nemognatha piazata (Fabricius) Meloidae Coleoptera - 4.3 Megachile rotundata Anthrax irroratus Say Bombyliidae Diptera + 24.2 Osmia caerulescens, + 24.3 Osmia pumila

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Figure Captions

Figure 1. A trap nest used to study cavity-nesting bees and wasps. The cardboard paper ‘nesting

tubes’ are inserted into a piece of pink insulation board fitted into a white PVC pipe for support

and protection from rain.

Figure 2. Variation in the mean emergence time for species of bee, wasp, and parasite recorded

from individuals taken from trap nests. ‘Taxa’ denotes cavity-nesting bees (B), cavity-nesting

wasps (W), and parasites (P). ‘Abd’ is the total number of individuals incubated and emerged

successfully. ‘Mean’ is the average number of days taken to emerge and ‘SE’ is the standard

error of the mean. Significant differences between species (‘sig’) were given alphabetically

where species sharing a letter were not significantly different from one another (α = 0.05). Those

species denoted with a “+” are considered introduced to the region.

Figure 3. Scatterplot illustrating a significantly positive community-wide correlation between

intraspecific mean and variation in emergence time.

Figure 4. Scatterplot showing the significant relationship between mean emergence time and

body size as measured by the intertegular width.

26